Abstracts
Migraine and vertigo are common disorders, with lifetime prevalences of 16% and 7% respectively, and co-morbidity around 3.2%. Vestibular syndromes and dizziness occur more frequently in migraine patients. We investigated bedside clinical signs indicative of vestibular dysfunction in migraineurs.
Objective
To test the hypothesis that vestibulo-ocular reflex, vestibulo-spinal reflex and fall risk (FR) responses as measured by 14 bedside tests are abnormal in migraineurs without vertigo, as compared with controls.
Method
Cross-sectional study including sixty individuals – thirty migraineurs, 25 women, 19-60 y-o; and 30 gender/age healthy paired controls.
Results
Migraineurs showed a tendency to perform worse in almost all tests, albeit only the Romberg tandem test was statistically different from controls. A combination of four abnormal tests better discriminated the two groups (93.3% specificity).
Conclusion
Migraine patients consistently showed abnormal vestibular bedside tests when compared with controls.
migraine; vertigo; bedside tests
Enxaqueca e vertigem são desordens comuns, com prevalência de 16% e 7% respectivamente, e comorbidade em torno de 3,2%. Síndromes vestibulares e tonturas ocorrem mais frequentemente em enxaquecosos. Pesquisamos alterações vestibulares utilizando testes de beira-de-leito em enxaquecosos.
Objetivo
Verificar se as respostas dos reflexos vestíbulo-ocular, vestíbulo-medular e risco de quedas medidas por 14 testes de beira-de-leito são diferentes comparando-se enxaquecosos sem vertigem, e controles.
Método
Estudo transversal com sessenta pessoas, 30 enxaquecosos; 25 mulheres, 19-60 anos; e trinta controles saudáveis pareados por sexo e idade.
Resultados
Houve tendência de pior desempenho entre enxaquecosos em quase todos testes, porém apenas o teste de Romberg tandem foi estatisticamente diferente dos controles. Uma combinação de quatro testes anormais discrimina os grupos com especificidade de 93,3%.
Conclusão
O grupo de enxaquecosos mostrou consistentemente testes vestibulares de beira-de-leito anormais quando comparados a controles.
enxaqueca; vertigem; testes de beira-de-leito
In neurological and otorrinolaryngological outpatients units migraine and vertigo are the two most common complains11. Brant T, Dieterich M, Strupp M. Vertigo and dizziness: common complains. London: Springer; 2009.. Vestibular syndromes, dizziness, vertiginous syndromes as benign positional paroxysmal vertigo, Ménière disease, motion sickness, cerebellar and anxiety disorders, in whom very often dizziness is present, all occur more frequently amongst migraineurs (30-50%)22. Shepard NT, Asher A. Non-vestibular dizziness and imbalance: suggestions for patients with migraine and mal de débarquement disequilibrium. In: Herdman SJ. Vestibular rehabilitation. 3rd ed. Philadelphia: E.A. Davis; 2007. p. 460-2. (Contemporary perspectives in rehabilitation).,33. Baier B, Winkenwerder E, Dieterich M. “Vestibular migraine”: effects of prophylactic therapy with various drugs: a restropective study. J Neurol 2009;256(3):436-42. doi:10.1007/s00415-009-0111-3,44. Lempert T, Neuhauser H. Epidemiology of vertigo, migraine and vestibular migraine. J Neurol. 2009;256(3):333-8. doi:10.1007/s00415-009-0149-2. It is well known that the equilibrium depends on an interplay between vestibular mechanisms, proprioception and visual inputs. Available data suggest that this circuitry could be dysfunctional in migraine. However, the issue as how, why and to which extent vestibular changes do occur in those subjects remains highly controversial. The objective of the present study was to test the hypothesis that bedside clinical tests specifically designed to detect subtle vestibular dysfunctions are abnormal in migraine in the absence of vestibular complains.
METHOD
In this cross sectional study, 30 (ICHD-2004, 2nd Ed. Cod:1; 1.1 and 1.2) interictal phase migraine patients, sequentially recruited in our unit and 30 matched healthy controls (patients partners and medical students) were blindly examined by the same researcher (ETM) after diagnosis. Inclusion and exclusion criteria were checked by well-trained neurologists with long headache expertise (PM-F and MBV). All tests 55. Halmagyi GM, Curthoys IS. A clinical sign of canal paresis. Arch Neurol. 1988;45(7):737-9. doi:10.1001/archneur.1988.00520310043015
6. Asawavichiangianda S, Fujimoto M., Mai M, Desroches H, Rutka J. Significance of head-shaking nystagmus in the evaluation of the dizzy patient. Acta Otolaryngol Suppl. 1999; 540:27-33. doi:10.1080/00016489950181152
7. Herdman SJ, Clendaniel RA. Vestibular rehabilitation. 4h ed. Philadelphia: FA Davis; 2014.
8. Zwergal A, Rettinger N, Frenzel C, Dieterich M, Brandt T, Strupp M. A bucket of static vestibular function. Neurology. 2009;7(19)2:1689-92. doi:10.1212/WNL.0b013e3181a55ecf
9. Linthicum Jr FH, Churchill D. Vestibular test results in acoustic tumor cases. Arch Otolaryng. 1968;88(6):604-7. doi:10.1001/archotol.1968.00770010606007
10. Shumway-Cook A, Horak FB. Assessing the influence of sensory interaction of balance: suggestion from the field. Phys Ther. 1986;66(10):1548-50.
11. Baloh RW, Honrubia V. Clinical neurophysiology of the vestibular system. 3rd ed. New York: Oxford University Press; 2001.
12. Barany R, 1910 apud Devin L, McCaslin, Dundas JA, Jacobson GP. The bedside assessment of the vestibular system. In: Jacobson GP, Shepard NT. Balance function assessment and management. San Diego: Plural; 2008. p. 90.
13. Fukuda T. The stepping test: two phases of the labyrinthine reflex. Acta Otolaryngol [Stockh]. 1959;50(1-2):95-108. doi:10.3109/00016485909129172
14. Podsiadlo D, Richardson S. The timed “up & go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc. 1991;39(2):142-8. doi:10.1111/j.1532-5415.1991.tb01616.x
15. Guralnik JM, Simonsick EM, Ferrucci L, Glynn RJ, Berkman LF et al. A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission. J Gerontol. 1994;49(2):M85-94. doi:10.1093/geronj/49.2.M85
16. Weiner DK, Duncan PW, Chandler J, Studenski SA. Functional reach: a marker of physical frailty. J Am Geriatr Soc. 1992;40(3):203-7. doi:10.1111/j.1532-5415.1992.tb02068.x
17. Shumway-Cook A, Baldwin M, Olissar NL, Gruber W. Predicting the probability of falls in community dwelling older adults. Phys Ther. 1997;77(8):812-9.-1818. Hall CD. Assessment of gait and balance. In: Herdman SJ, Clendaniel RA. Vestibular rehabilitation: a competency-based course. Atlanta: Emory Physical Therapy Association; 2010. (Table 1), were performed during one single session at the same hospital facility. Inclusion criteria were age between 18 and 65 years; migraine for at least 2 years with a minimum frequency of 2 attacks montly; and at least 1 brain Magnetic Ressonance (MRI) or Computerized Tomography (CT) scan within normal limits. Exclusion criteria were informed or clinically evidenced pregnancy; two or more tension-type headache episodes (ICHD-2004, 2nd Ed. Cod:2; 2.1, 2.2) in the previous week, chronic tension type headache (coded 2.3) or other headache listed in groups 3-4 (ICHD, 2004) according to clinical evaluation; circulatory, respiratory, orthopedic abnormalities or generalized weakness/tiredness of any nature which could influence/preclude the clinical tests; Ménière disease, vestibular neuritis, benign positional paroxysmal vertigo or phobic vertigo; spontaneous nystagmus; any sensitive, sensorineural, motor or coordination deficits; more than 150 mL coffee, 3 tea cups, or 2 soda cans intake per day for the last 2 days, or any amount of alcoholic beverages, tobacco, anti-vertiginous drugs, anti-depressive, anxiolytic antiemetic, or pain-killers more than b.i.d. use. All subjects underwent a neurootological examination including the minimal ice test (MIT)99. Linthicum Jr FH, Churchill D. Vestibular test results in acoustic tumor cases. Arch Otolaryng. 1968;88(6):604-7. doi:10.1001/archotol.1968.00770010606007. For the MIT a difference between right and left responses greater than 25% was considered as a canal paresis1919. Brandt T, Strupp M. General vestibular testing. Clin Neurophysiol. 2005;116(2):406-26. doi:10.1016/j.clinph.2004.08.009. The Wilcoxon Signed Rank, the McNemar chi-square, and the Student t test were used for statistical comparisons; p-values < 0.05 were considered significant. The local Ethics Committee approved this study (Protocol:159-11).
Tests for Vestibulo-ocular Reflex (VOR), Vestibulo-spinal Reflex (VSR) and fall risk (FR) used in clinical evaluation.
RESULTS
Participants were mostly females (83.3%). Migraine patients were aged 19-62 (median 39.3) years and controls 22-62 (median 38.9) years. Considering all tests together there was a clear tendency for migraineurs to perform worse than controls (p = 0.003), except for the SVV and the FRT (Table 2). The tests involving the vestibulo-ocular reflex (VOR) assessment (Figure 1) in general did not distinguish patients from healthy controls (p < 0.05).
Vestibulo-ocular reflex tests. Head impulse test (A, B, C); dynamic visual acuity (D, E); subjective visual vertical (F, G, H).
For the MIT the nystagmus duration ranged from 16 to 218 seconds in patients. The average percentage difference between R-L ears was 20.97 ± 15.9% in the patients group and 18 ± 11.5% in controls (Figure 2).
Vestibulo-spinal reflex tests. Past pointing (A, B, C); m-CTSIB step 4 (D); Fukuda test (E, F). fall risk: pull test (G).
Regarding the vestibulo-spinal reflex (VSR)(Figure 3), only the RTT was statistically different between the two groups (p = 0.039). For the the m-CTSIB, considering only the responses graded as 3 and 4, six migraine patients (20%) and three control subjects (10%) showed abnormal responses.
MIT. Patients and controls average nystagmus duration of caloric induced nystagmus in seconds. Box and whiskers plot showing the results of the MIT in seconds. Notice the grater response variability amongst patients. Box right (right ear), left (left ear).
The 5TSST and the PT tests were nearly statistically different (p = 0,074) in contrast with other Fall Risk (FR) tests.
A combination of 4 abnormal tests distinguish patients from controls with a sensitivity of 23.3% and a specificity of 93.3% (Table 3).
DISCUSSION
The present study shows that vertigo-free migraine patients, during the interictal phase, perform worse than controls in bedside clinical vestibular tests independently from vestibular complains.
Although various techniques may be used to address the vestibular function in migraine patients with or without vertigo2020. Bolay H, Bayazit YA, Gunduz B, Ugur AK, Akçali D, Altunyay S et al. Subclinical dysfunction of cochlea and cochlear efferents in migraine: an otoacoustic emission study. Cephalalgia. 2008;28(4):309-17. doi:10.1111/j.1468-2982.2008.01534.x
21. Dash AK, Panda N, Khandelwal G, Lal V, Mann SS. Migraine and audiovestibular dysfunction: is there a correlation? Am J Otolaryngol. 2008;29(5):295-99. doi:10.1016/j.amjoto.2007.09.004
22. Baier B, Stieber N, Dieterich M. Vestibular-evoked myogenic potentials in vestibular migraine. J Neurol. 2009;256(9):1447-54. doi:10.1007/s00415-009-5132-4
23. Arriaga MA, Chen DA, Hillman TA, Kunschner L, Arriaga RY. Visually enhanced vestibulo-ocular reflex: a diagnostic tool for migraine vestibulopathy. Laryngoscope. 2006;116(9):1577-9. doi:10.1097/01.mlg.0000231308.48145.f6
24. Çelebisoy N, Gokcay F, Sirin H, Biçak N. Migrainous vertigo: clinical, oculographic and posturographic findings. Cephalalgia. 2008;28(1):72-7. doi:10.1111/j.1468-2982.2007.01474.x-2525. Teggi R, Colombo B, Bernasconi L, Bellini C, Comi G, Bussi M. Migrainous vertigo: results of caloric testing and stabilometric findings. Headache. 2009;49(3):435-44. doi:10.1111/j.1526-4610.2009.01338.x, data considering vestibular bedside tests in this context are scarce.
Marcelli et al.2626. Marcelli V., Furia T., Marciano E. Vestibular pathways involvement in children with migraine: a neuro-otological study. Headache. 2010; 50(1):71-6. doi:10.1111/j.1526-4610.2009.01454.x evaluated otoneurological abnomalities in 22 migraineurs with vestibular symptoms as compared with 18 control migraineurs without vestibular symptoms. Seventy-three percent of the subjects in the first group had vestibular dysfunctions – peripheral, central or both – contrasting with 33% in the second group. The authors suggest the presence of a subclinical vestibular system involvement in the vertigo-free migraine patients.
Chronic headache causes postural instability, which could be the result of a sensory information rearrangement leading to greater vestibular system contribution paralleled by a reduced visual component in the equilibrium control2424. Çelebisoy N, Gokcay F, Sirin H, Biçak N. Migrainous vertigo: clinical, oculographic and posturographic findings. Cephalalgia. 2008;28(1):72-7. doi:10.1111/j.1468-2982.2007.01474.x. If this is true, migraineurs would be comparatively more dependent on vestibular functions for postural control, justifying the present results.
The tests we used to evaluate the VOR were not statistically different comparing the two groups. The response evoked by high accelerations (HIT) is controlled by a variety of different sensory and motor systems apart from the vestibular system. The VOR response can change within few minutes, pointing to a VOR plasticity77. Herdman SJ, Clendaniel RA. Vestibular rehabilitation. 4h ed. Philadelphia: FA Davis; 2014., but this is probably not sufficient to overcome the inadequate vestibular inputs and generate adequate responses. It is possible that chronic migraineurs develop the same phenomena identified in subjects with loss of vestibular function such as hidden saccades or other strategies to compensate a putative vestibular failure. Likewise, patients may increase the gain of the cervico-ocular reflex, and possibly the smooth pursuit system.
The DVA clearly tended to show worse results amongst patients although the SVV assessment was quite similar in both groups. Neck stiffness could putatively interfere with the DVA, as it has been shown that neck motility may be impaired in migraine2727. Tali D, Menahem I, Vered E, Kalichman L. Upper cervical mobility, posture and myofascial trigger points in subjects with episodic migraine: case-control study. J Bodyw Mov Ther. 2014;18(4):569-75. doi:10.1016/j.jbmt.2014.01.006.
MIT is a clean and quick monothermal bedside test, essentially a low-frequency stimulus caloric test that can detect vestibular impairment not apparent during higher-frequency head rotation2828. Schmäl F, Lübben B, Weiberg K, Stoll W. The minimal ice water caloric test compared with established vestibular caloric test procedures. J Vestib Res. 2005;15(4):215-24.,2929. Brevern M, Zeise D, Neuhauser H, Clarke AH, Lempert T. Acute migrainous vertigo: clinical and oculographic findings. Brain. 2005;128(2):365-74. doi:10.1093/brain/awh351. In accordance with the other tests, data also point to a vestibular instability in migraineurs, as reflected by a greater right-to-left asymmetry and a greater response spread amongst patients.
Apropos the VSR tests, Akdal et al.3030. Akdal G., Balci B. Evaluation of balance in vestibular migraine and migraine patients without history of vertigo. Neurology. 2013;80(meeting abstracts 1):261. carried out a balance and gait comparative study in 30 patients with vestibular migraine, 26 migraine without vertigo subjects, and 30 individuals whithout migraine. Among other tests and scales they also used the CTSIB and the DGI, concluding that vestibular migraine sufferers, defined according to the Lempert and Neuhauser criteria44. Lempert T, Neuhauser H. Epidemiology of vertigo, migraine and vestibular migraine. J Neurol. 2009;256(3):333-8. doi:10.1007/s00415-009-0149-2, as well as the migraineurs without vertigo, presented subnormal static and dynamic balance, as well as increased fall risk (FR). Góes3131. Góes CPQF. Avaliação do cerebelo na enxaqueca. Um estudo com estabilometria e ressonância magnética [thesis]. Rio de Janeiro: Universidade Federal do Rio de Janeiro; 2010. used a stabilometric test to assess the static equilibrium of migraine patients interictally. The stabilometric parameters did not differ between patients and controls. However, migraine with aura patients showed a significantly greater lateral oscillation than migraineurs without aura. In our study, the RTT was the most sensitive test, pointing to a dysfunction of the static equilibrium in migraineurs. Given the clearly unfavorable result for RTT it is possible that the dysfunction in migraine would be greater in the VSR mechanisms specially involving proprioceptive impulses. In the m-CTSIB test, when the subject is placed on the foam, the proprioceptive influence to the postural reflex drops by approximately 60%77. Herdman SJ, Clendaniel RA. Vestibular rehabilitation. 4h ed. Philadelphia: FA Davis; 2014.. Although the patients had no anteroposterior imbalance predominance, the migraneurs had three times more abnormal tests than controls, indicating that in migraine the vestibular influence on the posture control is comparatively dysfunctional. It remains to be explained wheather this is secondary to impaired neck and/or labyrith abnormal reflexes in migraine, as they could modulate the muscular tonus. Stretch reflexes receive important contribution from vestibulo-spinal responses, proprioceptive signs from the trunk and neck, or both, visual stimulus, and vonluntary responses3232. Davidoff RA. Skeletal muscle tone and the misunderstood stretch reflex. Neurology. 1992;42(5):951-63. doi:10.1212/WNL.42.5.951. Therefore, it is possible the subnormal vestibular function in migraine could increase the FR by stretch reflexes impairment.
In patients, the FR tests pointed to a subtle fall tendency. Only one patient showed increased FR according to the TUG test. Four migraneurs (13.3%), showed increased FR in the 5TSST, while none of the controls exceeded this test time limits (10 and 14.2 seconds, according to age). According to the FRT none of the sixty examined subjects showed an increased FR, indicating that the vestibular postural dysfunctions in migraine cannot be assessed by this test. Observing the FRT response in association with other vestibular-spinal tests we conclude that the anterior tilt does not seem to be particularly affected in migraine.
Given the clearly abnormal result for RTT in migraine patients, it is possible this disease impairs mainly VSR mechanisms, specially involving proprioceptive impulses. Since the RTT preferably tests a side-to-side control, our results are in line with the findings of Góes3131. Góes CPQF. Avaliação do cerebelo na enxaqueca. Um estudo com estabilometria e ressonância magnética [thesis]. Rio de Janeiro: Universidade Federal do Rio de Janeiro; 2010., in which the laleral oscillation was greater in migraineurs examined by stabilometry.
In the DGI, 13.3% of patients had a score of less than 19 points, i.e. suggestive of increased FR, while only one control (3.3%) scored for increased FR. Since this test requires different skills, it may be more sensitive than other FR assessment methods. The PT also shows that migraineurs present postural difficulties in the anteroposterior direction. The anticipatory postural reflexes are specially important in the anteroposterior instability provoked by pulling the patient. The corporal shift deterioration is an important factor for gait desarrangement in the elderly3333. Nutt JG, Marsden CD, Thompson PD. Human walking and higher-level gait disorders, particularly in the elderly. Neurology. 1993;43(2):268-79. doi:10.1212/WNL.43.2.268, but this cannot justify the comparatively worse PT results in migraineurs as they were not old. The anteroposterior instability in migraine seems to be better assessed by the PT than by the FRT.
The weaknesses of this work are the relatively small sample, the relatively lower age of patients for FR assessment, the lack of a migraine with vestibular symptoms group and other primary headache groups, and a lack of subsequent testing to confirm results consistency. Due to the high variation of the so-called “vestibular migraine” and the pathophysiological uncertainties related to this diagnosis we believe such patients cannot be selected by reliable criteria yet. Ideally, longitudinal and interventional studies specifically designed to assess vestibular dysfunction in migraine should be perfomed. However, we are confident data are convincing to demonstrate that migraineurs present subclinical vestibular dysfunctions that may be detected at the bedside. This is in line with the high prevalence of vertigo and unbalance complains amongst migraineurs.
In conclusion, migraine patients consistently showed worse vestibulo-ocular, vestibulo-spinal and FR bedside tests as compared with controls. The results indicate that the vestibular function is impaired subclinically in migraine without vertigo complains. Bedside tests are suitable to detect such dysfunctions. Whether these changes are specific for migraine headaches remains to be determined.
References
-
1Brant T, Dieterich M, Strupp M. Vertigo and dizziness: common complains. London: Springer; 2009.
-
2Shepard NT, Asher A. Non-vestibular dizziness and imbalance: suggestions for patients with migraine and mal de débarquement disequilibrium. In: Herdman SJ. Vestibular rehabilitation. 3rd ed. Philadelphia: E.A. Davis; 2007. p. 460-2. (Contemporary perspectives in rehabilitation).
-
3Baier B, Winkenwerder E, Dieterich M. “Vestibular migraine”: effects of prophylactic therapy with various drugs: a restropective study. J Neurol 2009;256(3):436-42. doi:10.1007/s00415-009-0111-3
-
4Lempert T, Neuhauser H. Epidemiology of vertigo, migraine and vestibular migraine. J Neurol. 2009;256(3):333-8. doi:10.1007/s00415-009-0149-2
-
5Halmagyi GM, Curthoys IS. A clinical sign of canal paresis. Arch Neurol. 1988;45(7):737-9. doi:10.1001/archneur.1988.00520310043015
-
6Asawavichiangianda S, Fujimoto M., Mai M, Desroches H, Rutka J. Significance of head-shaking nystagmus in the evaluation of the dizzy patient. Acta Otolaryngol Suppl. 1999; 540:27-33. doi:10.1080/00016489950181152
-
7Herdman SJ, Clendaniel RA. Vestibular rehabilitation. 4h ed. Philadelphia: FA Davis; 2014.
-
8Zwergal A, Rettinger N, Frenzel C, Dieterich M, Brandt T, Strupp M. A bucket of static vestibular function. Neurology. 2009;7(19)2:1689-92. doi:10.1212/WNL.0b013e3181a55ecf
-
9Linthicum Jr FH, Churchill D. Vestibular test results in acoustic tumor cases. Arch Otolaryng. 1968;88(6):604-7. doi:10.1001/archotol.1968.00770010606007
-
10Shumway-Cook A, Horak FB. Assessing the influence of sensory interaction of balance: suggestion from the field. Phys Ther. 1986;66(10):1548-50.
-
11Baloh RW, Honrubia V. Clinical neurophysiology of the vestibular system. 3rd ed. New York: Oxford University Press; 2001.
-
12Barany R, 1910 apud Devin L, McCaslin, Dundas JA, Jacobson GP. The bedside assessment of the vestibular system. In: Jacobson GP, Shepard NT. Balance function assessment and management. San Diego: Plural; 2008. p. 90.
-
13Fukuda T. The stepping test: two phases of the labyrinthine reflex. Acta Otolaryngol [Stockh]. 1959;50(1-2):95-108. doi:10.3109/00016485909129172
-
14Podsiadlo D, Richardson S. The timed “up & go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc. 1991;39(2):142-8. doi:10.1111/j.1532-5415.1991.tb01616.x
-
15Guralnik JM, Simonsick EM, Ferrucci L, Glynn RJ, Berkman LF et al. A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission. J Gerontol. 1994;49(2):M85-94. doi:10.1093/geronj/49.2.M85
-
16Weiner DK, Duncan PW, Chandler J, Studenski SA. Functional reach: a marker of physical frailty. J Am Geriatr Soc. 1992;40(3):203-7. doi:10.1111/j.1532-5415.1992.tb02068.x
-
17Shumway-Cook A, Baldwin M, Olissar NL, Gruber W. Predicting the probability of falls in community dwelling older adults. Phys Ther. 1997;77(8):812-9.
-
18Hall CD. Assessment of gait and balance. In: Herdman SJ, Clendaniel RA. Vestibular rehabilitation: a competency-based course. Atlanta: Emory Physical Therapy Association; 2010.
-
19Brandt T, Strupp M. General vestibular testing. Clin Neurophysiol. 2005;116(2):406-26. doi:10.1016/j.clinph.2004.08.009
-
20Bolay H, Bayazit YA, Gunduz B, Ugur AK, Akçali D, Altunyay S et al. Subclinical dysfunction of cochlea and cochlear efferents in migraine: an otoacoustic emission study. Cephalalgia. 2008;28(4):309-17. doi:10.1111/j.1468-2982.2008.01534.x
-
21Dash AK, Panda N, Khandelwal G, Lal V, Mann SS. Migraine and audiovestibular dysfunction: is there a correlation? Am J Otolaryngol. 2008;29(5):295-99. doi:10.1016/j.amjoto.2007.09.004
-
22Baier B, Stieber N, Dieterich M. Vestibular-evoked myogenic potentials in vestibular migraine. J Neurol. 2009;256(9):1447-54. doi:10.1007/s00415-009-5132-4
-
23Arriaga MA, Chen DA, Hillman TA, Kunschner L, Arriaga RY. Visually enhanced vestibulo-ocular reflex: a diagnostic tool for migraine vestibulopathy. Laryngoscope. 2006;116(9):1577-9. doi:10.1097/01.mlg.0000231308.48145.f6
-
24Çelebisoy N, Gokcay F, Sirin H, Biçak N. Migrainous vertigo: clinical, oculographic and posturographic findings. Cephalalgia. 2008;28(1):72-7. doi:10.1111/j.1468-2982.2007.01474.x
-
25Teggi R, Colombo B, Bernasconi L, Bellini C, Comi G, Bussi M. Migrainous vertigo: results of caloric testing and stabilometric findings. Headache. 2009;49(3):435-44. doi:10.1111/j.1526-4610.2009.01338.x
-
26Marcelli V., Furia T., Marciano E. Vestibular pathways involvement in children with migraine: a neuro-otological study. Headache. 2010; 50(1):71-6. doi:10.1111/j.1526-4610.2009.01454.x
-
27Tali D, Menahem I, Vered E, Kalichman L. Upper cervical mobility, posture and myofascial trigger points in subjects with episodic migraine: case-control study. J Bodyw Mov Ther. 2014;18(4):569-75. doi:10.1016/j.jbmt.2014.01.006
-
28Schmäl F, Lübben B, Weiberg K, Stoll W. The minimal ice water caloric test compared with established vestibular caloric test procedures. J Vestib Res. 2005;15(4):215-24.
-
29Brevern M, Zeise D, Neuhauser H, Clarke AH, Lempert T. Acute migrainous vertigo: clinical and oculographic findings. Brain. 2005;128(2):365-74. doi:10.1093/brain/awh351
-
30Akdal G., Balci B. Evaluation of balance in vestibular migraine and migraine patients without history of vertigo. Neurology. 2013;80(meeting abstracts 1):261.
-
31Góes CPQF. Avaliação do cerebelo na enxaqueca. Um estudo com estabilometria e ressonância magnética [thesis]. Rio de Janeiro: Universidade Federal do Rio de Janeiro; 2010.
-
32Davidoff RA. Skeletal muscle tone and the misunderstood stretch reflex. Neurology. 1992;42(5):951-63. doi:10.1212/WNL.42.5.951
-
33Nutt JG, Marsden CD, Thompson PD. Human walking and higher-level gait disorders, particularly in the elderly. Neurology. 1993;43(2):268-79. doi:10.1212/WNL.43.2.268
Publication Dates
-
Publication in this collection
20 Oct 2015 -
Date of issue
Jan 2016
History
-
Received
26 June 2015 -
Reviewed
12 Aug 2015 -
Accepted
01 Sept 2015